Metal oxidation states in biological water splitting

Krewald, Vera; Retegan, Marius; Cox, Nicholas; Messinger, Johannes; Lubitz, Wolfgang; DeBeer, Serena; Neese, Frank; Pantazis, Dimitrios A.

doi:10.1039/c4sc03720k

Cited by 285 publications

(515 citation statements)

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“…The S 4 state immediately relaxes to the S 0 state on release of O 2 . The oxidation states of the Mn atoms within the cluster have long been a source of debate, especially around whether the cluster exists in a high-oxidation [Mn(III) 2 Mn(IV) 2 ] or low-oxidation [Mn(III) 4 or Mn(II)Mn(III) 2 Mn(IV)] state in S 1 (8)(9)(10)(11)(12).…”

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confidence: 99%

“…With the information of atomic coordinates from high-resolution X-ray structures of the WOC, quantum chemical calculation is now a very powerful method in investigation of the water oxidation mechanism (10,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). Calculations using the density functional theory (DFT) and quantum mechanics/molecular mechanics (QM/MM) methods can be used to predict individual S-state structures and hence, the reaction scheme.…”

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confidence: 99%

“…Calculations using the density functional theory (DFT) and quantum mechanics/molecular mechanics (QM/MM) methods can be used to predict individual S-state structures and hence, the reaction scheme. Experimental data, such as EPR and extended X-ray absorption fine structure (EXAFS), as well as X-ray structural information were simulated using these methods to identify the protonation structure and the oxidation states (10,13,15,20,21), although a definite conclusion has not yet been reached.In contrast to EPR and EXAFS, which provide information mainly about the Mn 4 CaO 5 core, FTIR spectroscopy provides structural information about the protein moiety and water molecules coupled to the Mn 4 CaO 5 cluster (25-27). FTIR spectroscopy, which detects molecular vibrations, is highly sensitive to the structures and interactions of functional groups, and hence, the FTIR difference technique can recognize subtle structural changes at a much finer structural resolution than X-ray crystallography.…”

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Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Nakamura

Noguchi

2016

Proc. Natl. Acad. Sci. U.S.A.

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During photosynthesis, the light-driven oxidation of water performed by photosystem II (PSII) provides electrons necessary to fix CO 2 , in turn supporting life on Earth by liberating molecular oxygen. Recent high-resolution X-ray images of PSII show that the wateroxidizing center (WOC) is composed of an Mn 4 CaO 5 cluster with six carboxylate, one imidazole, and four water ligands. FTIR difference spectroscopy has shown significant structural changes of the WOC during the S-state cycle of water oxidation, especially within carboxylate groups. However, the roles that these carboxylate groups play in water oxidation as well as how they should be properly assigned in spectra are unresolved. In this study, we performed a normal mode analysis of the WOC using the quantum mechanics/ molecular mechanics (QM/MM) method to simulate FTIR difference spectra on the S 1 to S 2 transition in the carboxylate stretching region. By evaluating WOC models with different oxidation and protonation states, we determined that models of high-oxidation states, Mn(III) 2 Mn(IV) 2 , satisfactorily reproduced experimental spectra from intact and Ca-depleted PSII compared with low-oxidation models. It is further suggested that the carboxylate groups bridging Ca and Mn ions within this center tune the reactivity of water ligands bound to Ca by shifting charge via their π conjugation.T he oxidation of water, performed by photosystem II (PSII) in plants and cyanobacteria, is a crucial part of the photosynthesis process, providing a source of electrons used for CO 2 fixation. This process also produces molecular oxygen as a byproduct; this "waste" oxygen is released to the atmosphere, where it plays an essential role in sustaining life on Earth. The catalytic site of water oxidation is a water-oxidizing center (WOC) located in the electron-donor side of PSII (1-3). Recent high-resolution (1.9-1.95 Å) X-ray crystallographic structures of PSII (4, 5) revealed that the WOC core is an Mn 4 CaO 5 cluster fixed to the protein by six carboxylate [D1-D170, D1-E189, D1-E333, D1-D342, D1-A344 (C terminus), and CP43-E354] ligands and one imidazole (D1-H332) ligand. Four water ligands are also bound to Mn 4 (W1 and W2) and Ca (W3 and W4) (Fig. 1B shows numbering of the Mn ions and water ligands); several water molecules also exist around the Mn 4 CaO 5 cluster, forming a hydrogen bond network (Fig. 1A). Because of the absence of the information of hydrogen atoms in the X-ray structures, however, the protonation states of the water and oxo ligands in Mn 4 CaO 5 as well as the structure of the hydrogen bond network remain to be clarified.The water-oxidizing reaction proceeds through a cycle of five intermediates designated as S n states (n = 0−4) (6, 7), where S 1 is the most stable in the dark. Oxidation of the Mn 4 CaO 5 cluster by a Y Z • radical, produced by light-induced charge separation, advances the S n state (n = 0−3) to the S n + 1 state. The S 4 state immediately relaxes to the S 0 state on release of O 2 . The oxidation states of the Mn atoms wi...

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confidence: 99%

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confidence: 99%

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Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Nakamura

Noguchi

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Electron paramagnetic resonance (EPR) studies and high-resolution variants thereof have been at the forefront in revealing electronic level information about the intermediate states. 7 Even with high-resolution EPR methods, however, the assignment of hyperfine couplings (hfcs) to nuclear positions is often difficult and speculative. The utility of DFT calculations in assigning EPR hfcs for organic free radicals has been appreciated for some time.…”

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Manganese Oxidation State Assignment for Manganese Catalase

Beal

O’Malley

2016

J. Am. Chem. Soc.

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ABSTRACT:The oxidation state assignment of the manganese ions present in the superoxidized manganese (III/IV) catalase active site is determined by comparing experimental and broken symmetry density functional theory calculated 14 N, 17 O, and 1 H hyperfine couplings. Experimental results have been interpreted to indicate that the substrate water is coordinated to the Mn(III) ion. However, by calculating hyperfine couplings for both scenarios we show that water is coordinated to the Mn(IV) ion and that the assigned oxidation states of the two manganese ions present in the site are the opposite of that previously proposed based on experimental measurements alone.T he mechanism of water oxidation catalyzed by the oxygenevolving complex (OEC) of photosystem II (PSII) remains one of nature's great mysteries. Due in large part to the availability of accurate structural information obtained from recent high-resolution crystal structures, 1,2 the mechanism of water oxidation is gradually yielding its secrets. In addition to its fundamental biological importance, this knowledge is vital for developing future artificial photosynthetic devices capable of hydrogen production from water. 3−5 During the catalytic cycle, the OEC, comprising at its core a Mn 4 CaO 5 complex, cycles through five distinct oxidation states known as the S n states (where n = 0−4). 6 To fully understand water oxidation, it is necessary to obtain an understanding of the key intermediates and stages involved at both a structural and electronic level. This is a crucial step in the elucidation of plausible water oxidation mechanisms. Electron paramagnetic resonance (EPR) studies and high-resolution variants thereof have been at the forefront in revealing electronic level information about the intermediate states. 7 Even with high-resolution EPR methods, however, the assignment of hyperfine couplings (hfcs) to nuclear positions is often difficult and speculative. The utility of DFT calculations in assigning EPR hfcs for organic free radicals has been appreciated for some time. 8 More recent reports have demonstrated that for exchange coupled metal clusters such as the OEC, combined EPR and broken symmetry density functional theory (BS-DFT) calculations can be equally effective. 9 Manganese catalase, a dimanganese complex which catalyzes the disproportionation of hydrogen peroxide to water and molecular oxygen, has been proposed to be an evolutionary precursor of the OEC. 10,11 Additionally the active site of superoxidized manganese (III/IV) catalase, seen in Figure 1, has been used as a proteinaceous model of the S 2 state of the OEC. In contrast to the synthetic dimanganese complexes also used to model the OEC, superoxidized manganese catalase is able to mimic important features of the protein environment surrounding the OEC such as the coordination by protein side chains and a water molecule. 12,13 The di μ-oxo glutamate motif together with further glutamate and histidine ligation closely resembles the manganese ligation in the OEC. Although catalytic...

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Water oxidation in oxygenic photosynthesis studied by magnetic resonance techniques

2022

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The understanding of light‐induced biological water oxidation in oxygenic photosynthesis is of great importance both for biology and (bio)technological applications. The chemically difficult multistep reaction takes place at a unique protein‐bound tetra‐manganese/calcium cluster in photosystem II whose structure has been elucidated by X‐ray crystallography (Umena et al. Nature 2011, 473, 55). The cluster moves through several intermediate states in the catalytic cycle. A detailed understanding of these intermediates requires information about the spatial and electronic structure of the Mn4Ca complex; the latter is only available from spectroscopic techniques. Here, the important role of Electron Paramagnetic Resonance (EPR) and related double resonance techniques (ENDOR, EDNMR), complemented by quantum chemical calculations, is described. This has led to the elucidation of the cluster's redox and protonation states, the valence and spin states of the manganese ions and the interactions between them, and contributed substantially to the understanding of the role of the protein surrounding, as well as the binding and processing of the substrate water molecules, the O‐O bond formation and dioxygen release. Based on these data, models for the water oxidation cycle are developed.

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Metal oxidation states in biological water splitting

Abstract: A central question in biological water splitting concerns the oxidation states of the manganese ions that comprise the oxygen-evolving complex of photosystem II.

Cited by 285 publications

References 214 publications

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Manganese Oxidation State Assignment for Manganese Catalase

Water oxidation in oxygenic photosynthesis studied by magnetic resonance techniques

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Metal oxidation states in biological water splitting

Abstract: A central question in biological water splitting concerns the oxidation states of the manganese ions that comprise the oxygen-evolving complex of photosystem II.

Cited by 285 publications

References 214 publications

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn 4 CaO 5 cluster in photosystem II

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn 4 CaO 5 cluster in photosystem II

Manganese Oxidation State Assignment for Manganese Catalase

Water oxidation in oxygenic photosynthesis studied by magnetic resonance techniques

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Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn ₄ CaO ₅ cluster in photosystem II